The hormone prolactin is a novel, endogenous trophic factor able to regulate reactive glia and to limit retinal degeneration

Journal of Neuroscience

Volumn 34, Issue 5, 2014, Pages 1868-1878

  Arnold, Edith ^a   Thebault, Stéphanie ^a   Baeza Cruz, German ^a   Zamarripa, David Arredondo ^a   Adán, Norma ^a   Quintanar Stéphano, Andrés ^b   Condés Lara, Miguel ^a   Rojas Piloni, Gerardo ^a   Binart, Nadine ^c   de la Escalera, Gonzalo Martínez ^a   Clapp, Carmen ^a  

^a INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

^b UNIVERSIDAD AUTÓNOMA DE AGUASCALIENTES   (Mexico)

^c INSERM   (France)

Author keywords

Gliosis; Prolactin; Retinal degeneration; Trophic factor

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; PROLACTIN; PROLACTIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; ELECTRORETINOGRAPHY; FEMALE; GLIOSIS; HYPERPROLACTINEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RETINA CELL; RETINA DEGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION;

GLIOSIS; PROLACTIN; RETINAL DEGENERATION; TROPHIC FACTOR;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; FEMALE; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HYPERPROLACTINEMIA; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGHT; MALE; MICE; MICE, TRANSGENIC; NEUROGLIA; PROLACTIN; RATS; RATS, WISTAR; RECEPTORS, PROLACTIN; RETINAL DEGENERATION; RETINAL DISEASES; RNA, MESSENGER;

EID: 84893082320     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2452-13.2014     Document Type: Article

References (75)

1. Adler RA (1986) The anterior pituitary-grafted rat: a valid model of chronic hyperprolactinemia. Endocr Rev 7: 302-313. CrossRef Medline
2. Agha A, Rogers B, Mylotte D, Taleb F, Tormey W, Phillips J, Thompson CJ (2004) Neuroendocrine dysfunction in the acute phase of traumatic brain injury. Clin Endocrinol (Oxf) 60: 584-591. CrossRef
3. Allen DM, Cristy M (1978) Thiourea does not block visual pigment responses to prolactin in trout. Vision Res 18: 859-860. CrossRef Medline
4. Aranda J, Rivera JC, Jeziorski MC, Riesgo-Escovar J, Nava G, López-Barrera F, Quiróz-Mercado H, Berger P, Martínez de la Escalera G, Clapp C (2005) Prolactins are natural inhibitors of angiogenesis in the retina. Invest Ophthalmol Vis Sci 46: 2947-2953. CrossRef Medline
5. Azcoitia I, Santos-Galindo M, Arevalo MA, Garcia-Segura LM (2010) Role of astroglia in the neuroplastic and neuroprotective actions of estradiol. Eur J Neurosci 32: 1995-2002. CrossRef Medline
6. Babenko O, Golubov A, Ilnytskyy Y, Kovalchuk I, Metz GA (2012) Genomic and epigenomic responses to chronic stress involve miRNA-mediated programming. PLoS One 7: e29441. CrossRef Medline
7. Bailey JP, Nieport KM, Herbst MP, Srivastava S, Serra RA, Horseman ND (2004) Prolactin and transforming growth factor-beta signaling exert opposing effects on mammary gland morphogenesis, involution, and the Akt-forkhead pathway. Mol Endocrinol 18: 1171-1184. CrossRef Medline
8. Barres BA (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60: 430-440. CrossRef Medline
9. Benatti C, Valensisi C, Blom JM, Alboni S, Montanari C, Ferrari F, Tagliafico E, Mendlewicz J, Brunello N, Tascedda F (2012) Transcriptional profiles underlying vulnerability and resilience in rats exposed to an acute unavoidable stress. J Neurosci Res 90: 2103-2115. CrossRef Medline
10. Ben-Jonathan N, LaPensee CR, LaPensee EW (2008) What can we learn from rodents about prolactin in humans? Endocr Rev 29: 1-41. CrossRef Medline
11. Bhatnagar A, Ghauri AJ, Hope-Ross M, Lip PL (2009) Diabetic retinopathy in pregnancy. Curr Diabetes Rev 5: 151-156. CrossRef Medline
12. Binart N, Helloco C, Ormandy CJ, Barra J, Clément-Lacroix P, Baran N, Kelly PA (2000) Rescue of preimplantatory egg development and embryo implantation in prolactin receptor-deficient mice after progesterone administration. Endocrinology 141: 2691-2697. CrossRef Medline
13. Bringmann A, Reichenbach A (2001) Role of Muller cells in retinal degenerations. Front Biosci 6: E72-E92. CrossRef Medline
14. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A (2006) Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25: 397-424. CrossRef Medline
15. Bringmann A, Iandiev I, Pannicke T, Wurm A, Hollborn M, Wiedemann P, Osborne NN, Reichenbach A (2009) Cellular signaling and factors involved in Muller cell gliosis: neuroprotective and detrimental effects. Prog Retin Eye Res 28: 423-451. CrossRef Medline
16. Busik JV, Mohr S, Grant MB (2008) Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes 57: 1952-1965. CrossRef Medline
17. Caffé AR, Söderpalm A, van Veen T (1993) Photoreceptor-specific protein expression of mouse retina in organ culture and retardation of rd degeneration in vitro by a combination of basic fibroblast and nerve growth factors. Curr Eye Res 12: 719-726. CrossRef Medline
18. Chen A, Kumar SM, Sahley CL, Muller KJ (2000) Nitric oxide influences injury-induced microglial migration and accumulation in the leech CNS. J Neurosci 20: 1036-1043. Medline
19. Chioléro R, Lemarchand T, Schutz Y, de Tribolet N, Felber JP, Freeman J, Jéquier E (1988) Plasma pituitary hormone levels in severe trauma with or without head injury. J Trauma 28: 1368-1374. CrossRef Medline
20. Corbacho AM, Macotela Y, Nava G, Eiserich JP, Cross CE, Martínez de la Escalera G, Clapp C (2003) Cytokine induction of prolactin receptors mediates prolactin inhibition of nitric oxide synthesis in pulmonary fibroblasts. FEBS Lett 544: 171-175. CrossRef Medline
21. Corbacho AM, Valacchi G, Kubala L, Olano-Martín E, Schock BC, Kenny TP, Cross CE (2004) Tissue-specific gene expression of prolactin receptor in the acute-phase response induced by lipopolysaccharides. Am J Physiol Endocrinol Metab 287: E750-E757. CrossRef Medline
22. Crim JW (1975a) Prolactin-induced modification on visual pigments in the eastern red-spotted newt, Notophthalmus viridescens. Gen Comp Endocrinol 26: 233-242. CrossRef Medline
23. Crim JW (1975b) Prolactin-thyroxine antagonism and the metamorphosis of visual pigments in Rana catesbeiana tadpoles. J Exp Zool 192: 355-362. CrossRef Medline
24. Cruickshanks KJ, Klein R, Klein BE (1993) Sunlight and age-related macular degeneration. The Beaver Dam Eye Study. Arch Ophthalmol 111: 514-518. CrossRef Medline
25. De Luca Brunori I, Moggi G, Fornaro P, Teti G, Murru S, Gadducci A, Castrogiovanni P, Perossini M (1985) Evaluation of the central dopaminergic activity in gestational hyperprolactinaemia by means of the electroretinographic technique. Clin Exp Obstet Gynecol 12: 13-15. Medline
26. De Bellis A, Bizzarro A, Pivonello R, Lombardi G, Bellastella A (2005) Prolactin and autoimmunity. Pituitary 8: 25-30. CrossRef Medline
27. De Vito WJ, Stone S, Shamgochian M (1995) Prolactin induced expression of glial fibrillary acidic protein and tumor necrosis factor-alpha at a wound site in the rat brain. Mol Cell Endocrinol 108: 125-130. CrossRef Medline
28. Ding J, Sackmann-Sala L, Kopchick JJ (2013) Mouse models of growth hormone action and aging: a proteomic perspective. Proteomics 13: 674-685. CrossRef Medline
29. Dogusan Z, Hooghe R, Verdood P, Hooghe-Peters EL (2001) Cytokine-like effects of prolactin in human mononuclear and polymorphonuclear leukocytes. J Neuroimmunol 120: 58-66. CrossRef Medline
30. Dong CJ, Agey P, Hare WA (2004) Origins of the electroretinogram oscillatory potentials in the rabbit retina. Vis Neurosci 21: 533-543. CrossRef Medline
31. Fontaine V, Kinkl N, Sahel J, Dreyfus H, Hicks D (1998) Survival of purified rat photoreceptors in vitro is stimulated directly by fibroblast growth factor-2. J Neurosci 18: 9662-9672. Medline
32. Grieshaber MC, Moramarco F, Schoetzau A, Flammer J, Orguel S (2012) Detection of retinal glial cell activation in glaucoma by time domain optical coherence tomography. Klin Monbl Augenheilkd 229: 314-318. CrossRef Medline
33. Grosche J, Härtig W, Reichenbach A (1995) Expression of glial fibrillary acidic protein (GFAP), glutamine synthetase (GS), and Bcl-2 protooncogene protein by Muller (glial) cells in retinal light damage of rats. Neurosci Lett 185: 119-122. CrossRef Medline
34. Harada T, Harada C, Nakayama N, Okuyama S, Yoshida K, Kohsaka S, Matsuda H, Wada K (2000) Modification of glial-neuronal cell interactions prevents photoreceptor apoptosis during light-induced retinal degeneration. Neuron 26: 533-541. CrossRef Medline
35. Harada T, Harada C, Kohsaka S, Wada E, Yoshida K, Ohno S, Mamada H, Tanaka K, Parada LF, Wada K (2002) Microglia-Müller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci 22: 9228-9236. Medline
36. Huang X, Hui MN, Liu Y, Yuen DS, Zhang Y, Chan WY, Lin HR, Cheng SH, Cheng CH (2009) Discovery of a novel prolactin in non-mammalian vertebrates: evolutionary perspectives and its involvement in teleost retina development. PLoS One 4: e6163. CrossRef Medline
37. Joly S, Lange C, Thiersch M, Samardzija M, Grimm C (2008) Leukemia inhibitory factor extends the lifespan of injured photoreceptors in vivo. J Neurosci 28: 13765-13774. CrossRef Medline
38. Jones BW, Watt CB, Frederick JM, Baehr W, Chen CK, Levine EM, Milam AH, Lavail MM, Marc RE (2003) Retinal remodeling triggered by photoreceptor degenerations. J Comp Neurol 464: 1-16. CrossRef Medline
39. Kolomeyer AM, Sugino IK, Zarbin MA (2013) Characterization of the effects of retinal pigment epithelium-conditioned media on porcine and aged human retina. Graefes Arch Clin Exp Ophthalmol 251: 1515-1528. CrossRef Medline
40. Langmann T (2007) Microglia activation in retinal degeneration. J Leukoc Biol 81: 1345-1351. CrossRef Medline
41. Larinkari J, Laatikainen L, Ranta T, Mörönen P, Pesonen K, Laatikainen T (1982) Metabolic control and serum hormone levels in relation to retinopathy in diabetic pregnancy. Diabetologia 22: 327-332. CrossRef Medline
42. La Vail MM, Yasumura D, Matthes MT, Lau-Villacorta C, Unoki K, Sung CH, Steinberg RH (1998) Protection of mouse photoreceptors by survival factors in retinal degenerations. Invest Ophthalmol Vis Sci 39: 592-602. Medline
43. Leff MA, Buckley DJ, Krumenacker JS, Reed JC, Miyashita T, Buckley AR (1996) Rapid modulation of the apoptosis regulatory genes, bcl-2 and bax by prolactin in rat Nb2 lymphoma cells. Endocrinology 137: 5456-5462. CrossRef Medline
44. Marc RE, Jones BW, Watt CB, Vazquez-Chona F, Vaughan DK, Organisciak DT (2008) Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis 14: 782-806. Medline
45. Möderscheim TA, Gorba T, Pathipati P, Kokay IC, Grattan DR, Williams CE, Scheepens A (2007) Prolactin is involved in glial responses following a focal injury to the juvenile rat brain. Neuroscience 145: 963-973. CrossRef Medline
46. Moloney JB, Drury MI (1982) The effect of pregnancy on the natural course of diabetic retinopathy. Am J Ophthalmol 93: 745-756. Medline
47. Morales T (2011) Recent findings on neuroprotection against excitotoxicity in the hippocampus of female rats. J Neuroendocrinol 23: 994-1001. CrossRef Medline
48. Nag TC, Wadhwa S (2012) Ultrastructure of the human retina in aging and various pathological states. Micron 43: 759-781. CrossRef Medline
49. Olafson RP, O'Steen WK (1976) Hormonal influences on photoreceptor damage: the pituitary gland and ovaries. Invest Ophthalmol 15: 869-872. Medline
50. Organisciak DT, Vaughan DK (2010) Retinal light damage: mechanisms and protection. Prog Retin Eye Res 29: 113-134. CrossRef Medline
51. Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, Edery M, Brousse N, Babinet C, Binart N, Kelly PA (1997) Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 11: 167-178. CrossRef Medline
52. O'Steen WK, Kraeer SL (1977) Effects of hypophysectomy, pituitary gland homogenates and transplants, and prolactin on photoreceptor destruction. Invest Ophthalmol Vis Sci 16: 940-946. Medline
53. O'Steen WK, Sundberg DK (1982) Patterns of radioactivity in the eyes of rats after injection of iodinated prolactin. Ophthalmic Res 14: 54-62. CrossRef Medline
54. Popeski N, Amir S, Woodside B (1999) Changes in NADPH-d staining in the paraventricular and supraoptic nuclei during pregnancy and lactation in rats: role of ovarian steroids and oxytocin. J Neuroendocrinol 11: 53-61. CrossRef Medline
55. Quiambao AB, Tan E, Chang S, Komori N, Naash MI, Peachey NS, Matsumoto H, Ucker DS, Al-Ubaidi MR (2001) Transgenic Bcl-2 expressed in photoreceptor cells confers both death-sparing and death-inducing effects. Exp Eye Res 73: 711-721. CrossRef Medline
56. Rangaswamy NV, Zhou W, Harwerth RS, Frishman LJ (2006) Effect of experimental glaucoma in primates on oscillatory potentials of the slowsequence mfERG. Invest Ophthalmol Vis Sci 47: 753-767. CrossRef Medline
57. Raso GM, Meli R, Gualillo O, Pacilio M, Di Carlo R (1999) Prolactin induction of nitric oxide synthase in rat C6 glioma cells. J Neurochem 73: 2272-2277. CrossRef Medline
58. Rattner A, Nathans J (2005) The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. J Neurosci 25: 4540-4549. CrossRef Medline
59. Rivera JC, Aranda J, Riesgo J, Nava G, Thebault S, López-Barrera F, Ramírez M, Martínez de la Escalera G, Clapp C (2008) Expression and cellular localization of prolactin and the prolactin receptor in mammalian retina. Exp Eye Res 86: 314-321. CrossRef Medline
60. Sanes JR, Zipursky SL (2010) Design principles of insect and vertebrate visual systems. Neuron 66: 15-36. CrossRef Medline
61. Simard AR, Rivest S (2007) Neuroprotective effects of resident microglia following acute brain injury. J Comp Neurol 504: 716-729. CrossRef Medline
62. Takamiya Y, Kohsaka S, Toya S, Otani M, Tsukada Y (1988) Immunohistochemical studies on the proliferation of reactive astrocytes and the expression of cytoskeletal proteins following brain injury in rats. Brain Res 466: 201-210. Medline
63. Tanaka T, Shiu RP, Gout PW, Beer CT, Noble RL, Friesen HG (1980) A new sensitive and specific bioassay for lactogenic hormones: measurement of prolactin and growth hormone in human serum. J Clin Endocrinol Metab 51: 1058-1063. CrossRef Medline
64. Tessier C, Prigent-Tessier A, Ferguson-Gottschall S, Gu Y, Gibori G (2001) PRL antiapoptotic effect in the rat decidua involves the PI3K/protein kinase B-mediated inhibition of caspase-3 activity. Endocrinology 142: 4086-4094. CrossRef Medline
65. Unterlauft JD, Eichler W, Kuhne K, Yang XM, Yafai Y, Wiedemann P, Reichenbach A, Claudepierre T (2012) Pigment epithelium-derived factor released by Muller glial cells exerts neuroprotective effects on retinal ganglion cells. Neurochem Res 37: 1524-1533. CrossRef Medline
66. Vega C, Moreno-Carranza B, Zamorano M, Quintanar-Stéphano A, Méndez I, Thebault S, Martínez de la Escalera G, Clapp C (2010) Prolactin promotes oxytocin and vasopressin release by activating neuronal nitric oxide synthase in the supraoptic and paraventricular nuclei. Am J Physiol Regul Integr Comp Physiol 299: R1701-R1708. CrossRef Medline
67. Wachtmeister L (1998) Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res 17: 485-521. CrossRef Medline
68. Wahlin KJ, Campochiaro PA, Zack DJ, Adler R (2000) Neurotrophic factors cause activation of intracellular signaling pathways in Muller cells and other cells of the inner retina, but not photoreceptors. Invest Ophthalmol Vis Sci 41: 927-936. Medline
69. Walter P, Widder RA, Lüke C, Königsfeld P, Brunner R (1999) Electrophysiological abnormalities in age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 237: 962-968. CrossRef Medline
70. Wässle H (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5: 747-757. CrossRef Medline
71. Wen R, Tao W, Li Y, Sieving PA (2012) CNTFand retina. Prog Retin Eye Res 31: 136-151. CrossRef Medline
72. Wexler EM, Berkovich O, Nawy S (1998) Role of the low-affinity NGF receptor (p75) in survival of retinal bipolar cells. Vis Neurosci 15: 211-218. CrossRef Medline
73. Zack DJ (2000) Neurotrophic rescue of photoreceptors: are Muller cells the mediators of survival? Neuron 26: 285-286. CrossRef Medline
74. Zhang K, Zhang L, Weinreb RN (2012a) Ophthalmic drug discovery: novel targets and mechanisms for retinal diseases and glaucoma. Nat Rev Drug Discov 11: 541-559. CrossRef Medline
75. Zhang M, Xu G, Liu W, Ni Y, Zhou W (2012b) Role of fractalkine/CX3CR1 interaction in light-induced photoreceptor degeneration through regulating retinal microglial activation and migration. PLoS One 7: e35446. CrossRef Medline